Abstract
Morphogenesis in animal tissues is largely driven by actomyosin networks, through tensions generated by an active contractile process. Although the network components and their properties are known, and networks can be reconstituted in vitro, the requirements for contractility are still poorly understood. Here, we describe a theory that predicts whether an isotropic network will contract, expand, or conserve its dimensions. This analytical theory correctly predicts the behavior of simulated networks, consisting of filaments with varying combinations of connectors, and reveals conditions under which networks of rigid filaments are either contractile or expansile. Our results suggest that pulsatility is an intrinsic behavior of contractile networks if the filaments are not stable but turn over. The theory offers a unifying framework to think about mechanisms of contractions or expansion. It provides the foundation for studying a broad range of processes involving cytoskeletal networks and a basis for designing synthetic networks.
Highlights
Networks of cytoskeletal filaments display a variety of behaviors
But we still lack an intuitive understanding of how they come about, as it is difficult to extrapolate between the microscopic level, where filaments are moved by molecular motors and restrained by crosslinking elements, and the level of the entire system
Small networks can be studied with computer simulations (Mendes Pinto et al, 2012; Stachowiak et al, 2014; Oelz et al, 2015; Ennomani et al, 2016; Hiraiwa & Salbreux, 2016), but we lack a simpler approach that can make rapid predictions purely based on analytical deduction. Such a theoretical framework would be valuable to classify the different behaviors that are seen experimentally. In search for such a general theory, we chose initially to concentrate on the major factor determining contraction of networks, that is the force created by molecular motors, we recognized that filament shortening could lead to contractility (Backouche et al, 2006; Mendes Pinto et al, 2012; Oelz et al, 2015)
Summary
Networks of cytoskeletal filaments display a variety of behaviors. A decisive feature for the physiological role of networks is whether they contract or expand. Small networks can be studied with computer simulations (Mendes Pinto et al, 2012; Stachowiak et al, 2014; Oelz et al, 2015; Ennomani et al, 2016; Hiraiwa & Salbreux, 2016), but we lack a simpler approach that can make rapid predictions purely based on analytical deduction Such a theoretical framework would be valuable to classify the different behaviors that are seen experimentally. In search for such a general theory, we chose initially to concentrate on the major factor determining contraction of networks, that is the force created by molecular motors, we recognized that filament shortening could lead to contractility (Backouche et al, 2006; Mendes Pinto et al, 2012; Oelz et al, 2015). We show that contractile systems become pulsatile if filament turnover is introduced in the model
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